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Diet Induced Changes in the Microbiota and Cell Composition of Rabbit Gut Associated Lymphoid Tissue (GALT)

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Diet Induced Changes in the Microbiota and Cell Composition of Rabbit Gut Associated Lymphoid Tissue (GALT) www.nature.com/scientificreports OPEN Diet induced changes in the microbiota and cell composition of rabbit gut associated lymphoid Received: 10 May 2018 Accepted: 10 September 2018 tissue (GALT) Published: xx xx xxxx Rakel Arrazuria 1, Valentín Pérez2, Elena Molina1, Ramón A. Juste1,5, Ehsan Khafpour3,4 & Natalia Elguezabal1 The gut associated lymphoid tissue (GALT) is the largest immune organ of the body. Although the gut transient and mucosa-associated microbiota have been largely studied, the microbiota that colonizes the GALT has received less attention. The gut microbiome plays an important role in competitive exclusion of pathogens and in development and maturation of immunity. Diet is a key factor afecting the microbiota composition in the digestive tract. To investigate the relation between diet, microbiota and GALT, microbial and cell composition of vermiform appendix (VA) and sacculus rotundus (SR) were studied in two groups of New Zealand white rabbits on diferent diets. Diet shifted the lymphoid tissue microbiota afecting the presence and/or absence of certain taxa and their abundances. Immunohistochemistry revealed that a higher fbre content diet resulted in M cell hyperplasia and an increase of recently recruited macrophages, whereas T-cell levels remained unaltered in animals on both high fbre and standard diets. These fndings indicate that diet has an impact on the microbiota and cell composition of the GALT, which could act as an important microbial recognition site where interactions with benefcial bacteria can take place favouring microbiota replacement after digestive dysregulations. Te gut associated lymphoid tissue (GALT) is the largest immune organ of the body. It is a well-developed com- ponent of the mucosal immune system that is involved in protection of the host against pathogens and in the postnatal immune system maturation1. In rabbits the structure of the GALT is even more developed than in other mammalian species2. Te rabbit possesses two organized lymphoid tissue diferentiated segments or organs: the sacculus rotundus (SR), which is located at the distal end of the ileum, forming the ileo-cecal junction, and the vermiform appendix (VA), located at the end of the cecum and that is considered an immune structure primarily functioning as a safe-house for ben- efcial bacteria3. Tese two lymphoid organs account for more than 50% of the total lymphoid tissue in the rabbit4. Te gut microbiota plays an important role in the development and maturation of intestinal mucosal immu- nity5 and contributes to the health of the host by colonizing the mucosal entry sites of pathogens. Moreover, the microbiota mediates resistance to infection indirectly by stimulating the innate immune response6. Many stud- ies have documented diferences in the composition of host associated microbial communities between healthy and diseased states7,8. It is recognized that an altered microbiome is not just a marker of disease but that it also actively contributes to pathogenesis9. According to the current knowledge on the cecal appendix function as ‘a “safe-house” for benefcial bacteria with the capacity to re-inoculate the gut following depletion of the normal fora afer diarrheal illness’3, its microbiota has an even more important role in the health of the individual. In the last decade, the great development of next generation sequencing technologies, has enabled researchers to investigate the digestive microbial composition under diferent conditions. However, although the gut transient and mucosa-associated microbiota have been largely studied, little is known about the microbiota that specifcally 1Department of Animal Health, NEIKER-Instituto Vasco de Investigación y Desarrollo Agrario, Derio, Bizkaia, Spain. 2Department of Animal Health, Faculty of Veterinary Medicine, University of Leon, Leon, Spain. 3Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada. 4Department of Medical Microbiology, University of Manitoba, Winnipeg, MB, Canada. 5Present address: SERIDA, Agri-food Research and Development Regional Service, Villaviciosa, Asturias, Spain. Correspondence and requests for materials should be addressed to N.E. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:14103 | DOI:10.1038/s41598-018-32484-1 1 www.nature.com/scientificreports/ colonizes the GALT which is directly interacting with the immune system. It has been demonstrated that specifc microbial profle on vermiform appendix can induce infammation10. Diet has a major impact on health and it could be used in the near future as an alternative approach to control infammatory and autoimmune diseases11. Diet is also one of the key factors afecting the composition of the microbiota in the digestive tract12 since dietary nutrients are the principal substrates for the microbial popu- lations. Finally, diet can also have a direct efect on the immune response since food components beyond their function as nutrients, can play an important role in the operation of the immune system in health and disease13. In the last years, many studies have documented the benefts of high fbre diets on human health, based on the production of short-chain fatty acids (SCFA) by the microbiota as a consequence of fbre degradation14. Te predominant SCFAs are known to reduce the production of pro-infammatory cytokines15 and recruit Treg cells as well as induce the expression of antimicrobial peptides16. Fibre based diets, have been shown to pro- mote and increase gut microbiota diversity17 and also to diminish infammatory responses by a mechanism that includes shaping the intestinal microbiome and indirectly afecting the immune system18. Moreover, a dietary fbre-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility19. Te efect of diet in experimental infection models in mice20 and rabbits21 has been studied, highlighting the impor- tance of diet in experimental trials involving animals. In addition to the diffuse lymphoid tissue formed by infiltrating cells interspersed at different densities throughout the regular mucosa, the GALT is formed by highly organized structures enclosed in the mucosal layer of the intestinal wall. Tese structures are formed by a lymphoid follicle covered by a dome of epithelial cells. Most of these epithelial cells are those known as M (microfold or membranous) cells. M cells play an important role in the transport of antigens from the lumen of the intestine to mucosal lymphoid tissues in which the processing and initiation of immune responses occur22. Antigens acquired by M cells are rapidly shuttled via vesicular transport to the basolateral membrane where they are released, enabling uptake by antigen presenting cells and processing for presentation to T cells23. Recently, it has been discovered that M cells have a critical role in the establishment of normal secretory immunity at GALT sites23. Moreover, it has been reported that dietary fbre and starch levels are related to the size and number of M cells in rabbit lymphoid tissue24. In the rabbit, approximately 50% of the overlying epithelial cells are M cells whereas in in rats and humans only 5–10% of them are M cells2. Te biological signifcance of this diference remains unknown. Recent studies focused on the characterization of rabbit GALT have concluded that rabbits are comparable to humans through- out their GALT supporting the use of the rabbit model to study human gut-associated disease or orally acquired infectious agents25. Moreover, SR and VA are highly diferentiated areas that may be the reservoir from which microbiota replacement would start afer digestive dysregulations3. Diet, microbiota and immunity are highly connected, but our understanding of how this network functions is still limited. Because dietary fbre intake has demonstrated health benefts, the objective of this study was to assess the efect of a high fbre diet on microbiota and cell composition using the rabbit GALT model. Results Growth performance. Animal weight (Supplementary Fig. S2 and Table S2a) of Diet group A was signif- icantly higher at the frst three timepoints (weeks 0, 7 and 11). Weight increase among groups across diferent intervals (Supplementary Table 2b) did not show signifcant diferences except for intervals 20–24 and 20–27 weeks where Diet B animals showed lower weight increase. Total weight increase (31–0 week) among groups did not show signifcant diferences. Microbiota analysis. Afer quality control and removal of chimeric reads, an average of 22,657 (SD = 9,055) high quality sequences were obtained for downstream analyses. Te rarefaction curve built with the observed species (Richness) showed asymptotic tendency (Supplementary Fig. S3), which indicates that the sampling efort was sufcient to compare species numbers. Diversity analysis of the SR and VA samples revealed no signifcant diferences in richness (Chao 1 index), or other alpha-diversity indices (Shannon and Simpson) between animals on diet A and B (Supplementary Fig. S4). Te beta-diversity analysis of UniFrac distances revealed distinct clustering pattern between animals on diet A and B in both weighted (p = 0.049) and unweighted (p = 0.036) measures (Fig. 1a,b). However, when the dis- tances between SR and VA were analyzed, no signifcant diferences were observed in weighted (p = 0.764) and unweighted (p = 0.886) measures. Moreover, no interactions were detected between sampled tissue and diet when weighted (p = 0.341) and unweighted (p = 0.6414) distances measures were analyzed
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